Massive mitochondrial DNA content in diplonemid and kinetoplastid protists

Abstract

SummaryThe mitochondrial DNA of diplonemid and kinetoplastid protists is known for its suite of bizarre features, including the presence of concatenated circular molecules, extensive trans‐splicing and various forms of RNA editing. Here we report on the existence of another remarkable characteristic: hyper‐inflated DNA content. We estimated the total amount of mitochondrial DNA in four kinetoplastid species (Trypanosoma brucei, Trypanoplasma borreli, Cryptobia helicis, and Perkinsela sp.) and the diplonemid Diplonema papillatum. Staining with 4′,6‐diamidino‐2‐phenylindole and RedDot1 followed by color deconvolution and quantification revealed massive inflation in the total amount of DNA in their organelles. This was further confirmed by electron microscopy. The most extreme case is the ∼260 Mbp of DNA in the mitochondrion of Diplonema, which greatly exceeds that in its nucleus; this is, to our knowledge, the largest amount of DNA described in any organelle. Perkinsela sp. has a total mitochondrial DNA content ~6.6× greater than its nuclear genome. This mass of DNA occupies most of the volume of the Perkinsela cell, despite the fact that it contains only six protein‐coding genes. Why so much DNA? We propose that these bloated mitochondrial DNAs accumulated by a ratchet‐like process. Despite their excessive nature, the synthesis and maintenance of these mtDNAs must incur a relatively low cost, considering that diplonemids are one of the most ubiquitous and speciose protist groups in the ocean. © 2018 The Authors. IUBMB Life published by Wiley Periodicals, Inc. on behalf of International Union of Biochemistry and Molecular Biology., 70(12):1267–1274, 2018

Mitochondrial genetics revisited

“…The loss of mtDNA is viable in some yeast species but not all (Fekete, Cierna, Poláková, Piskur, & Sulo, ) and is a source of speciation in trypanosomes (Lai, Hashimi, Lun, Ayala, & Lukes, ). Conversely, the amplification of mtDNA in some species of Diplonemids or Kinetoplastids can be such that its total amount largely exceeds that of nuclear DNA (Lukes, Wheeler, Jirsova, David, & Archibald, ). This eccentric genetic component of eukaryotic cells exhibits a great architectural diversity across the tree of life (Smith & Keeling, ), and although the numerous mitochondrial genomes now sequenced give us an impression of exhaustive knowledge (http://www.ncbi.nlm.nih.gov/genome.organelle/), new surprises are not excluded as novel evolutionary branches will be explored.…”

Comparative molecular cell biology of phototrophic euglenids and parasitic trypanosomatids sheds light on the ancestor of Euglenozoa

“…The kinetoplastids and diplonemids contain the largest amounts of mitochondrial DNA found to date in eukaryotes, often exceeding the amount of nuclear DNA. The approximately 260 Mb of DNA in the diplonemid D. papillatum mitochondria is the largest amount of mitochondrial DNA found in a eukaryote and is approximately 80 Mb more than the amount of nuclear DNA (Lukeš et al, ). The basal endosymbiotic bodonid, Perkinsela sp., has approximately 6.6 times more mitochondrial than nuclear DNA (Lukeš et al, ).…”

“…The approximately 260 Mb of DNA in the diplonemid D. papillatum mitochondria is the largest amount of mitochondrial DNA found in a eukaryote and is approximately 80 Mb more than the amount of nuclear DNA (Lukeš et al, ). The basal endosymbiotic bodonid, Perkinsela sp., has approximately 6.6 times more mitochondrial than nuclear DNA (Lukeš et al, ). In comparison, the mitochondrial DNA of the bodonid Trypanoplasma borreli and trypanosomatid T. brucei comprises approximately 50% and 5% of total DNA, respectively (Lukeš et al, ).…”

“…The basal endosymbiotic bodonid, Perkinsela sp., has approximately 6.6 times more mitochondrial than nuclear DNA (Lukeš et al, ). In comparison, the mitochondrial DNA of the bodonid Trypanoplasma borreli and trypanosomatid T. brucei comprises approximately 50% and 5% of total DNA, respectively (Lukeš et al, ). The mitochondrial DNA content of euglenids is currently unknown, but it is assumed that it is similar to that found in most eukaryotes.…”

“…The mitochondrial DNA content of euglenids is currently unknown, but it is assumed that it is similar to that found in most eukaryotes. Based on this assumption, it has been proposed that mitochondrial DNA content rapidly increased in the common ancestor of diplonemids and kinetoplastids soon after divergence from euglenids (Lukeš et al, ).…”